Molekularny mechanizm endoreduplikacji u roślin wyższych

• Authors: Monika Rewers

Title variants

EN

Molecular mechanism of endoreduplication in higher plants

• Languages of publication: PL EN

Abstracts

PL

Proces endoreduplikacji stanowi alternatywną formę cyklu komórkowego, podczas której następuje amplifikacja jądrowego DNA, po której nie zachodzi jednak mitoza i podział komórki. Mechanizm molekularny tego procesu w dużej mierze opiera się na białkach uczestniczących w typowym cyklu komórkowym i polega na zablokowaniu mitozy wraz z ponownym zainicjowaniem replikacji DNA. W endoreduplikacji ważną rolę odgrywają kinazy zależne od cyklin oraz ich białka regulatorowe - cykliny. Podczas tego procesu aktywność tych białek jest regulowana na poziomie transkrypcyjnym i potranslacyjnym. Zmiana aktywności kinaz zależnych od cyklin może wynikać ze zmniejszenia dostępności cyklin w wyniku zablokowania ich transkrypcji oraz ze zmian statusu fosforylacji kinaz zależnych od cyklin. Może być również negatywnie regulowana poprzez fosforylację podjednostki kinazy zależnej od cyklin przez kinazę WEE1 oraz poprzez interakcję z inhibitorami kinaz zależnych od cyklin. Regulacja na poziomie potranslacyjnym polega natomiast na ukierunkowanej destrukcji cyklin przez kompleks promujący anafazę/cyklosom. Szczegółowe omówienie mechanizmów molekularnych tego procesu zostało przedstawione w poniższym artykule.

EN

Endoreduplication represents an alternative form of the cell cycle in which nuclear DNA amplification occurs, but it is not followed by mitosis and cell division. The molecular mechanism of this process is largely based on proteins involved in typical cell cycle and involves block of mitosis and re-initiation of DNA replication. Cyclin-dependent kinases and theirs regulatory proteins - cyclins are the key components of endoreduplication. During the process, activity of these proteins is regulated at the transcriptional and post-translational levels. Changes in the activity of cyclin dependent kinases may be due to a reduced availability of cyclins resulting from blocking of respective genes transcription and to changes in the status of cyclin-dependent phosphorylation of kinases. It can be also negatively regulated by phosphorylation of the cyclin-dependent kinase subunit by kinase WEE1, and by interaction with inhibitors of cyclin dependent kinases. Post-translational regulation occurs via targeted destruction of cyclins by the anaphase promoting complex/cyclosome. A detailed discussion of the molecular mechanism of these processes is presented in this article.

Keywords

PL

CDK; cykliny; endocykl; endopoliploidalność; polisomatyczność

EN

CDK; cyclins; endocycle; endopolyploidy; polysomaty

• Journal: Kosmos
• Year: 2017
• Volume: 66
• Issue: 3
• Pages: 475-485

Dates

published

2017

Contributors

author

Monika Rewers

• Zakład Biologii Molekularnej i Cytometrii, Katedra Genetyki, Fizjologii i Biotechnologii Roślin, Uniwersytet Technologiczno-Przyrodniczy, im. Jana i Jędrzeja Śniadeckich w Bydgoszczy, Al. Prof. S. Kaliskiego 7, 85-796 Bydgoszcz, Polska
• Laboratory of Molecular Biology and Cytometry, Department of Plant Genetics, Physiology and Biotechnology, UTP University of Science and Technology, Kaliskiego Ave. 7, 85-796 Bydgoszcz, Poland

References

• Baloban M., Vanstraelen M., Tarayre S., Reuzeau C., Cultrone A., Mergaert P., Kondorosi E., 2013. Complementary and dose-dependent action of AtCCS52A isoforms in endoreduplication and plant size control. New Phytol. 198, 1049-1059.
• Barow M., Meister A., 2003. Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell, Environ. 26, 571-584.
• Bisbis B., Delmas F., Joubés J., Sicard A., Hernould M., Inzé D., Mouras A., Chevalier C., 2006. Cyclin-dependent kinase (CDK) inhibitors regulate the CDK-Cyclin complex activities in endoreduplicating cells of developing tomato fruit. J. Biol. Chem. 281, 7374-7383.
• Boniotti M. B., Griffith M. E., 2002. 'Cross-talk' between cell division cycle and development in plants. Plant Cell 14, 11-16.
• Bramsiepe J., Wester K., Weinl C., Roodbarkelari F., Kasili R., Larkin J. C., Hülskamp M., Schnittger A., 2010. Endoreduplication controls cell fate maintenance. PLoS Genet. 6, e1000996.
• Breuer C., Ishida T., Sugimoto K., 2010. Developmental control of endocycles and cell growth in plants. Curr. Opin. Plant Biol. 13, 654-660.
• Breuer C., Braidwood L., Sugimoto K., 2014. Endocycling in the path of plant development. Curr. Opin. Plant Biol. 17, 78-85.
• Cebolla A., Vinardell J. M., Kiss E., Oláh B., Roudier F., Kondorosi A., Kondorosi E., 1999. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 18, 4476-4484.
• Chevalier C., Nafati M., Methieu-Rivet E., Bpurdon M., Frangne N., Cheniclet C., Renaudin J.-P., Gévaudant F., Hernould M., 2011. Elucidating the functional role of endoreduplication in tomato fruit development. Ann. Bot. 107, 1159-1169.
• Churchman M. L., Brown M. L., Kato N., Kirik V., Hülskamp M., Inzé D., De Veylder L., Walker J. D., Zheng Z., Oppenheimer D. G., Gwin T., Churchman J., Larkin J. C., 2006. SIAMESE, a plant-specific cell cycle regulator, controls endoreduplication onset in Arabidopsis thaliana. Plant Cell 18, 3145-3157.
• Cook G. S., Lentz Grønlund A., Siciliano I., Spadafora N., Amini M., Herbert R. J., Bitonti M. B., Graumann K., Francis D., Rogers H. J., 2013. Plant WEE1 kinase is cell cycle regulated and removed at mitosis via the 26S proteasome machinery. J. Exp. Bot. 64, 2093-2106.
• D'Amato F., 1984. Role of polyploidy in reproductive organs and tissue. [W:] Embryology of angiosperms. Johrii B. M (red.). Springer, Berlin/Heidelberg/New York, 519-566.
• De Almeida Engler J., De Veylder L., De Groodt R., Rombauts S., Boudolf V., De Mayer B., Hemerly A., Ferreira P., Beeckman T., Karimi M., Hilson P., Inzé D., Engler G., 2009. Systematic analysis of cell-cycle gene expression during Arabidopsis development. Plant J. 59, 645-660.
• Deckert J., 2000. Regulacja genów cyklu komórkowego roślin. Wydawnictwo Naukowe UAM, Poznań.
• De Schutter K., Joubés J., Cools T., Verkest A., Corellou F., Babiychuk E., Van Der Schueren Beeckman T., Kushnir S., Inzé D., De Veylder L., 2007. Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19, 211-225.
• De Veylder L., Beeckman T., Beemster G. T. S., Krols L., Terras F., Landrieu I., Van Der Schueren E., Maes S., Naudts M., Inzé D., 2001. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13, 1653-1668.
• De Veylder L., Joubés J., Inzé D., 2003. Plant cell cycle transitions. Curr. Opin. Plant Biol. 6, 536-543.
• De Veylder L., Larkin J. C., Schnittger A., 2011. Molecular control and function of endoreduplication in development and physiology. Trends Plant Sci. 16, 624-634.
• Dissmeyer N., Weimer A. K., Pusch S., De Schutter K., Alvim Kamei C. L., Nowack M. K., Novak B., Duan G. L., Zhu Y. G., De Veylder L., Schnittger A., 2009. Control of cell proliferation, organ growth, and DNA damage response operate independently of dephosphorylation of the Arabidopsis Cdk1 homolog CDKA;1. Plant Cell 19, 3641-3654.
• Eloy N. B., Gonzalez N., Van Leene J., Maleux K., Vanhaeren H., De Milde L., Dhondt S., Vercruysse L., Witters E., Mercier R., Cromer L., Beemster G. T. S., Remaut H., Van Montagu M. C. E., De Jaeger G., Ferreira P. C. G., Inzé D., 2012. SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization. Proc. Natl. Acad. Sci. USA 13853-13858.
• Eloy N. B., de Freitas Lima M., Ferreira P. C.G., Inzé D., 2015. The Role of the Anaphase-Promoting Complex/Cyclosome in Plant Growth. Crit. Rev. Plant Sci. 34, 487-505.
• Gonzalez N., Hernould M., Delmas F., Gévaudant F., Duffe P., Causse M., Mouras A., Chevalier C., 2004. Molecular characterization of a WEE1 gene homologue in tomato (Lycopersicon esculentum Mill.). Plant Mol. Biol. 56, 849-861.
• González-Sama A., Coba de la Pena T., Kevei Z., Mergaert P., Lucas M. M., de Felipe M. R., Kondorosi E., Pueyo J. J., 2006. Nuclear DNA endoreduplication and expression of the mitotic inhibitor Ccs52 associated to determine and lupinoid nodule organogenesis. Mol. Plant-Microbe Interact. 19, 173-180.
• Gonzalez N., Gévaudant F., Hernould M., Chevalier C., Mouras A., 2007. The cell cycle-associated protein kinase WEE1 regulates cell size in relation to endoreduplication in developing tomato fruit. Plant J. 51, 642-655.
• Heyman J., De Veylder L., 2012. The Anaphase-Promoting Complex/Cyclosome in control of plant development. Mol. Plant 5, 1182-1194.
• Imai K. K., Ohashi Y., Tsuge T., Yoshizumi T., Matsui M., Oka A., Aoyama T., 2006. The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18, 382-396.
• Inzé D., De Veylder L., 2006. Cell cycle regulation in plant development. Ann. Rev. Genet. 40, 77-105.
• John P. C. L., Qi R., 2008. Cell division and endoreduplication: doubtful engines of vegetative growth. Trends Plant Sci. 13, 121-127.
• Joubés J., Chevalier C., 2000. Endoreduplication in higher plants. Plant Mol. Biol. 43, 737-747.
• Kasili R., Walker J. D., Simmons L. A., Zhou J., De Veylder L., Larkin J. C., 2010. SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes. Genetics 185, 257-268.
• Kirik V., Schrader A., Uhrig J. F., Hulskamp M., 2007. MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing. Plant Cell 19, 3100-3110.
• Krawczyk J., Wąsek I., 2011. Endoreduplikacja jako jeden z mechanizmów zmiany ilości jądrowego DNA w komórce roślinnej. Wiadomości Botaniczne 55, 7-22.
• Kudo N., Kimura Y., 2001. Flow cytometric evidence for endopolyploidy in seedlings of some Brassica species. Theor. Appl. Genet. 102, 104-110.
• Larson-Rabin Z., Li Z., Masson P. H., Day C. D., 2009. FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol. 149, 874-884.
• Li C., Potuschak T., Colón-Carmona A., Gutiérrez R., Doerner P., 2005. Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc. Natl. Acad. Sci. USA 102, 12978-12983.
• Li Z.-Y., Li B., Dong A.-W., 2012. The Arabidopsis transcription factor AtTCP15 regulates endoreduplication by modulating expression of key cell cycle genes. Mol. Plant 5, 270-280.
• Lima M. de F., Eloy N. B., Pegoraro C., Sagit R., Rojas C., Bretz T., Vargas L., Elofsson A., Costa de Oliveira A., Hemerly A. S., Ferreira P. C. G., 2010. Genomic evolution and complexity of the Anaphase-Promoting Complex (APC) in land plants. BMC Plant Biol. 10, 254.
• Mathieu-Rivet E., Gévaudant F., Chenicklet C., Hernould M., Chevalier C., 2010. The anaphase promoting complex activator CCS52A, a key factor for fruit growth and endoreduplication in tomato. Plant Signaling Behav. 5, 985-987.
• Małuszynska J., Kolano B., Sas-Nowosielska H., 2013. Endopoliploidy in plants. [W:] Plant genome diversity. Physical structure, behaviour and evolution of plant genomes. Leich I. J. (red.). Springer-Verlag Wien 2, 99-119.
• Mishiba K., Mii M., 2000. Polysomaty analysis in diploid and tetraploid Portulaca grandiflora. Plant Sci. 156, 213-219.
• Nagl W., 1976. DNA endoreduplication and polyteny understood as evolutionary strategies. Nature 261, 614-615.
• Okello R. C. O., de Visser P. H. B., Heuvelink E., Marcelis L. F. M., Struik P. C., 2016. Light mediated regulation of cell division, endoreduplication and cell expansion. Environ. Exp. Bot. 121, 39-47.
• Ormenese S., De Almeida Engler J., De Groodt R., De Veylder L., Inzé D., Jacqmard A., 2004. Analysis of the spatial expression pattern of seven Kip Related Proteins (KRPs) in the shoot apex of Arabidopsis thaliana. Ann. Bot. 93, 575-580.
• Rewers M., Śliwińska E., 2012. Endoreduplication intensity as a marker of seed developmental stage in the Fabaceae. Cytometry Part A 81, 1067-1075.
• Rewers M., Śliwińska E., 2014. Endoreduplication in the germinating embryo and young seedling is related to the type of seedling establishment but is not coupled with superoxide radical accumulation. J. Exp. Bot. 65, 4385-4396.
• Sabelli P. A., Larkins B. A., 2009. Regulation and function of retinoblastoma-related plant genes. Plant Sci. 177, 540-548.
• Schnittger A., Schöbinger U., Stierhof Y-D., Hülskamp M., 2002. Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr. Biol. 12, 415-420.
• Smulders M. J. M., Rus-Korteekas W., Gilissen L. J. W. 1994. Development of polysomaty during differentiation in diploid and tetraploid tomato (Lycopersicon esculentum) plants. Plant Sci. 97, 53-60.
• Sugimoto-Shirasu K., Roberts K., 2003. 'Big it up': endoreduplication and cell-size control in plants. Curr. Opin. Plant Biol. 6, 554-553.
• Sun Y., Flannigan B. A., Setter T. L., 1999a. Regulation of endoreduplication in maize (Zea mays L.) endosperm. Isolation of a novel B1-type cyclin and its quantitative analysis. Plant Mol. Biol. 41, 245-258.
• Sun Y., Dilkes B. P., Zhang C., Dante R. A., Carneiro N. P., Lowe K. S., Jung R., Gordon-Kamm W. J., Larkins B. A., 1999b. Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc. Natl. Acad. Sci. USA 96, 4180-4185.
• Śliwińska E., 2008. Zastosowanie cytometrii przepływowej do oznaczania DNA zawartości DNA u roślin. Post. Biol. Kom. 35, 165-176.
• Śliwińska E., Łukaszewska E., 2005. Polysomaty in growing in vitro sugar beet (Beta vulgaris) seedlings of different ploidy level. Plant Sci. 168, 1067-1074.
• Vandepoele K., Raes J., De Veylder L., Rouze P., Rombauts S., Inzé D., 2002. Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14, 903-916.
• Vanstraelen M., Baloban M., Da Ines O., Cultrone A., Lammens T., Boudolf V., Brown S.C., De Veylder L.,Mergaert P., Kondorosi E., 2009. APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl. Acad. Sci. USA 106, 11806-11811.
• Vinardell J. M., Fedorova E., Cebolla A., Kevei Z., Horvath G., Kelemen Z., Tarayre S., Roudier F., Mergaert P., Kondorosi A., Kondorosi E., 2003. Endoreduplication mediated by the Anaphase-Promoting Complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15, 2093-2105.
• Walker J. D., Oppenheimer D. G., Concienne J., Larkin J. C., 2000. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127, 3931-3940.
• Wang G., Kong H., Sun Y., Zhang X., Zhang W., Altman N., dePamphilis C. W. Ma H., 2004. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol. 135, 1084-1099.
• Wang H., Zhou Y., Torres-Acosta L., Fowke L. C., 2007. CDK inhibitors. [W:] Cell cycle control and plant development. Inzé D. (red.). Blackwell Publishing, Oxford, 62-86.
• Wang H., Zhou Y., Bird D. A., Fowke L. C., 2008. Functions, regulations and cellular localization of plant cyclin-dependent kinase inhibitors. J. Microsc. 231, 234-246.
• Weinl C., Marquardt S., Kuijt S. J. H., Nowack M. K., Jakoby M. J., Hülskamp M., Schnittger A., 2005. Novel functions of plant Cyclin-Dependent Kinase Inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 17, 1704-1722.